ORTHOCARDIINAE, Schneider, 2002

Schneider, Jay A., 2002, Phylogeny of cardiid bivalves (cockles and giant clams): revision of the Cardiinae and the importance of fossils in explaining disjunct biogeographical distributions, Zoological Journal of the Linnean Society 136 (3), pp. 321-369 : 352-359

ORTHOCARDIINAE

Orthocardiinae seems to be home to a disproportionate number of little studied and poorly understood generic-level taxa. Previous studies have tried to ally individual orthocardiine generic-level taxa with Acanthocardia , Bucardium , Vepricardium , and even Fraginae or the laevicardiine Nemocardium . It has not previously been considered that these taxa may together form a monophyletic group distinct from previously recognized subfamilies.

Europicardium was erected as a subgenus of Bucardium by Popov (1977) for several species of Oligocene to Pliocene cardiids from Europe and North Africa (see Schneider, 1998a; for the problems regarding the alleged Eocene Europicardium ). Keen (1980) classified Europicardium as a subgenus of Acanthocardia . These species had usually been classified as Trachycardium (see synonomy list in Ben Moussa, 1994); Ben Moussa (1994), Kókay (1985, 1996) and Monegatti & Raffi, 2001) still persisted in assigning species of Europicardium to Trachycardium, and erroneously argued that Trachycardium was once a component of Cenozoic to Recent faunas of Europe and the eastern Atlantic.

All of the most parsimonious trees from the present analysis indicate that Europicardium and Loxocardium are sister taxa, in a different clade ( Orthocardiinae ) than Bucardium and Acanthocardia (Cardiinae) . Juvenile specimens of Europicardium have nearly the exact shell shape of adult Loxocardium ( Fig. 23 ). It is therefore suggested that Europicardium evolved via peramorphosis from some species of Loxocardium ( Loxocardium thus being paraphyletic), or from a common ancestor of the two taxa, for the adult morphology of Europicardium has developed beyond that of its ancestor ( McNamara, 1986). Popov (1977) thought that Europicardium was extinct, but Cardium caparti Nickles, 1955 from west Africa has been placed in Europicardium by von Cosel (pers. comm. in Vidal, 1999). Von Cosel (pers. comm. in Vidal, 1999) also places another west African species, Cardium serrulatum Deshayes, 1855 , in Europicardium , but this species is herein considered a Trachycardium (Schneider, unpubl.). T. serrulata , from the Pleistocene and Recent of west Africa, is the only species of Trachycardium, fossil or Recent, from the eastern Atlantic (Schneider, unpubl.). Popov (1977) classified the Pleistocene to Recent Cardium sueziense Issel, 1869 as the sole living species of Loxocardium . Investigation of the shell and anatomy of this species (Schneider, unpubl.) indicates that C. sueziense is a species of the fragine Microfragum . There are no known living species of Loxocardium . A list of all valid Recent and fossil species of Europicardium may be found in Table 6.

Marwick (1944) erected the genus Hedecardium for several Eocene to Miocene cardiids from New Zealand and Australia. Just as numerous workers had used Trachycardium as a default taxon for the medium to large, heavily ornamented species that Popov (1977) would eventually place in Europicardium , many of the species that Marwick (1944) placed in Hedecardium had been classified as Trachycardium ( Suter, 1907, 1915; Powell & Bartrum, 1929; Laws, 1933) because of their medium to large size and prominent radial ribs.

Marwick (1944) first suggested that Hedecardium was allied with Vepricardium , but later ( Marwick, 1960) suggested that Hedecardium may be related to Nemocardium (Pratulum) . Beu & Maxwell (1990) adopted Marwick’s (1960) latter view, for both Nemocardium and Hedecardium have well-defined posterior slopes. As Marwick (1944), Maxwell (1978) and Beu & Maxwell (1990) indicated, the posterior ribs on Hedecardium are lower and more rounded than those on the rest of the shell. However, this ribbing pattern is the opposite of that seen on Nemocardium . On Nemocardium , the posterior ribs are more prominent than the ribs on the rest of the shell ( Dall, 1900; Keen, 1969a, 1980; Kafanov & Popov, 1977; Schneider, 1995; numerous others), although on some subgenera (including Pratulum) the anterior and central ribs increase in strength during ontogeny to be equal (or nearly so) in strength to the posterior ribs. On Hedecardium , the posterior ribs decrease in strength during ontogeny ( Figs 10A , 26 ). A decrease in strength of posterior ribs, coupled with a differentiation of the posterior slope of the shell, occurs independently in the cardiine Dinocardium , the laevicardiine Laevicardium & Clinocardiinae . Keen (1951, 1969a, 1980) considered Dinocardium , Laevicardium , Cerastoderma – now known to be the most basal lymnocardiine – ( Popov, 1977; Kafanov & Popov, 1977; Schneider, 1998b; numerous others) and the taxa now in Clinocardiinae to be a monophyletic group based primarily on the character of weakened posterior ribs. It has been shown that these taxa have evolved this condition independently ( Kafanov, 1974, 1980; Kafanov & Popov, 1977; Schneider, 1992).

An examination of Hedecardium (Iheringicardium) sheds further light on the relationship of Hedecardium s.l. to Orthocardiinae as opposed to Nemocardium . As is typical for eucardiids, H. (Iheringicardium) ameghinoi has spines along the tops of ribs all across the exterior of the shell, not just on the posterior, as on Hedecardium s.s. (see Figs 10A , 26 , 27 ). The only species of Nemocardium which have spines on the central and anterior slopes belong to the tiny, highly ornamented Neogene taxa Nemocardium (Trifaricardium) and N. ( Frigidocardium ); the closely related N. ( Microcardium ) has spines on the central slope ( Keen, 1969a, 1980; Wilson & Stevenson, 1977; Poutiers, 1992; Schneider, 1995). However, N. (Pratulum), from which Marwick (1960) and Beu & Maxwell (1990) derive Hedecardium s.l., has spines on the posterior slope only. Furthermore, some or all taxa of Hedecardium s.l. display eucardiid features unknown in Nemocardium : (1) all three subgenera of Hedecardium have cross-striae (2) primary radial threads are present on H. s.s and H. (Iheringicardium) ( Figs 26 , 27 ) and (3) secondary radial threads are present on H. (I) patagonicum ( Ihering, 1907) ( Fig. 27 ). Finally, as on virtually all Cenozoic eucardiids, the ribs on Hedecardium – especially the most basal taxon H. (Iheringicardium) – are very wide, usually wider than high ( Figs 10 , 26 and 27 ). However, the ribs of virtually all species of Nemocardium are very narrow, usually no wider than they are high ( Schneider, 1995, 1998a).

The increase in rib width on Cenozoic eucardiids relative to Cretaceous eucardiids (such as Granocardium ) and noneucardiids (such as Nemocardium ) has been shown to be the result of fusion of two adjacent ribs to form a single rib ( Schneider, 1998a). A radial rib on a Cenozoic eucardiid is therefore homologous to two radial ribs plus the intervening interspace on Granocardium or Nemocardium . The two sides of a rib on a Cenozoic eucardiid are each homologous to a single rib on Granocardium or Nemocardium , and the rib top on a Cenozoic eucardiid is homologous to the intervening interspace on Granocardium or Nemocardium .

Hedecardium (Iheringicardium) exhibits a further doubled rib. Scale in cm indicated on figure.

case of fusion of radial ribs. Fusion of pairs of radial ribs on the posterior slope of H. (I) philippii ( Ihering, 1897) has been described and figured by Ihering (1897: 249–250, pl. 6, fig. 40); an example of doubled ribs on this species is illustrated herein ( Fig. 26B ). Ortmann (1902) noted the same phenomenon. Ihering also described and figured fusion of radial rib pairs all along the exterior of H. (I) ameghinoi ( Ihering, 1907, p. 292, pl. 11, fig. 72a; see Fig. 27C, D , herein). Fusion of radial ribs also occurs on H. (I) patagonicum (pers. obs.). These doubled ribs clearly bear two rows of spines along the top of the rib. Each one of these doubled ribs on H. (Iheringicardium) therefore would be homologous to four radial ribs and three intervening interspaces on Granocardium or Nemocardium .

Hedecardium (Iheringicardium) is a South American endemic whose closest relatives ( Hedecardium s.s and H. [Titanocardium]) are known mostly from New Zealand ( Table 7). Marwick (1944), when erecting Hedecardium , suggested that the Australian species Cardium pseudomagnum McCoy, 1877 belonged to Hedecardium . Keen, who classified Hedecardium as a subgenus of Vepricardium , gave the biogeographical range of Hedecardium to be New Zealand, Australia and Burma ( Keen, 1969a) and later ( Keen, 1980) as South Pacific and South Asia. A thorough search of Keen’s unpublished notes in the NMNH yielded no species ever reported from Burma which she assigned to Hedecardium . The most likely source of Keen’s record of a Burmese Hedecardium is Cardium kanleanum Cotter, 1923 , which she called ‘ Vepricardium ??’ in her notes; I assign this species to Hedecardium s.s. ( Table 7) on the basis of its shell shape, slight umbonal ridge, and numerous (48–50) unornamented or weakly ornamented radial ribs. Darragh (1970) assigned C. moniletectum Tate, 1887 and C. septuagenarium Tate, 1887 to Hedecardium (but assigned C. pseudomagnum to Trachycardium); C. septuagenarium is herein considered a junior synonym of C. moniletectum . Most recently, Maxwell (1978; Beu & Maxwell, 1990) considered Hedecardium to be endemic to New Zealand.

It was von Ihering (1891) himself who noted the similarity between the faunas of New Zealand and South America, before he began working on South American Cenozoic molluscs. According to Ihering (1907), only six of the 282 molluscan species from the ‘Formation Pan-Patagonienne’ of Argentina (roughly equivalent to the Oligocene; see Olivera, Zinsmeister & Parma, 1994; references therein) were also recorded from New Zealand. It is uncertain whether Ihering ever associated the South American species herein placed in H. (Iheringicardium) with those now placed in either of the predominantly New Zealand taxa Hedecardium s.s. or H. (Titanocardium). However, the New Zealand geologist F. W. Hutton may have recognized some connection between the Tertiary cardiids of New Zealand and South America, for while discussing Cardium philippii Ihering, 1897 (a species now placed in H. [Iheringicardium]; Table 7), Ihering (1907) compared it with a New Zealand form sent to him by Hutton, which Hutton had identified (in writing to Ihering) as Cardium multistriatum Sowerby, 1833 . C. multistriatum is a name with a tortuous taxonomic history (see Fischer-Piette, 1977). Originally described from Recent shells from the Pacific coast of South America, Sowerby (1846) subsequently reported C. multistriatum from Tertiary material collected by Charles Darwin in Patagonia. Sowerby’s figure (Pl. II, fig. 16) is indeterminable. Ihering (1907: 291) said the New Zealand form was very different (“bien different[e]”) from both C. philippii and C. multistriatum and gave it the new name C. huttoni ; Powell & Bartrum (1929) would eventually synonomize C. huttoni with Cardium greyi Hutton, 1873 , which was placed in H. (Titanocardium) by Maxwell (1978). In short, there may have been even more evidence for a South America-New Zealand biogeographical connection than von Ihering (1891) thought, and the material was literally in his hands. None of the publications by Marwick, Beu or Maxwell concerning Hedecardium posit any relations with South American taxa.

Comparatively little attention has been paid to South American Oligocene and Lower Miocene molluscan faunas since Ihering (1907); the only references I know of to any of the cardiids herein assigned to H. (Iheringicardium) since Ihering (1907) have been compendia ( Ihering, 1914; Parodiz, 1996). It is predicted that a renewed study of the morphology and systematics of Oligocene and Miocene South American molluscs will demonstrate that the biogeographical relations between South America and New Zealand are stronger than currently thought, and that many taxa which have long been considered to be endemic to New Zealand actually may have representatives in South America.

The phylogenetic relationships of Agnocardia , Afrocardium and the species herein assigned to the new genus Freneixicardia likewise have been poorly understood. Stewart (1930) erected Agnocardia as a subgenus of Trachycardium. The species that Stewart assigned to Agnocardia had previously been placed in Trachycardium ( Conrad, 1865; Aldrich, 1911) or Acanthocardia ( Woodring, 1925; Gardner, 1926), primarily on the basis of the prominent spines. Keen (1951, 1969a, 1980) considered Agnocardia a subgenus of Acanthocardia . Popov (1977) classified Agnocardia as a subgenus of Bucardium . Agnocardia was raised to a genus by Vokes (1977; also see Vokes, 1984, 1989) and followed by Dockery (1982) and Schneider (1998a). Afrocardium was erected as a subgenus of Fragum by le Tomlin (1931). Keen (1951, 1969a, 1980) classified Afrocardium as a subgenus of the fragine Ctenocardia on the basis of Afrocardium ’s heavy tubular spines. Popov (1977) synonymized Afrocardium with Plagiocardium ; Kafanov and Popov (1977) placed Afrocardium in the subfamily Fraginae , tribe Parvicardiini , along with Parvicardium , Papillicardium (fragines; Schneider, 1998b), Plagiocardium , Maoricardium (basal members of the CFTL lineage, Schneider, 1998b), and Loxocardium (orthocardiine, herein). Kafanov & Popov (1977) also tentatively included in their new tribe Parvicardiini the Sarmatian (late Middle Miocene) brackish-water cardiids Inaequicostata , Kubanocardium and Obsoletiforma , which have more recently been considered lymnocardiines ( Nevesskaia et al., 1993; Paramonova, 1994). Cardium verrucosum and C. hausmanni , the species herein assigned to the new genus Freneixicardia , have previously been placed in Vepricardium ( Sacco, 1899; Cossmann, 1905; Glibert & Poel, 1970; Glibert, 1980; numerous others); however, Strougo (1976) and Popov (1977) did place C. verrucosum in Agnocardia .

As stated in Results, Agnocardia , Afrocardium and Freneixicardia share two synapomorphies with the other Orthocardiinae : spines entirely microstructurally discontinuous with the outer shell layer and a fully reflected maximum ventral shell margin. None of these three taxa has a crenulate posterior margin, the synapomorphy of Cardiinae s.s. Alternate tree topologies positing Agnocardia as a member of the Cardiinae s.s. add between five and 14 steps to the shortest trees. It is more parsimonious to consider Agnocardia a member of Orthocardiinae than Cardiinae . One of the three characters uniting Agnocardia and Afrocardium , concave ribs, is otherwise only known in Orthocardium and polymorphically in Hedecardium s.s. Positing Orthocardium as the sister taxon to Agnocardia + Afrocardium adds one step to the shortest trees. Positing Orthocardium as the sister taxon to Freneixicardia + ( Agnocardia + Afrocardium ), and thus reversal to convex or flat ribs in Freneixicardia , does not add any steps to the shortest trees.

Afrocardium is a member of the Orthocardiinae clearly closely related to Agnocardia (united by three characters in 92% of the shortest trees; see Results). Afrocardium does not possess any of the derived characters of Fraginae , including loss of the perisiphonal suture (see Schneider, 1998b). There may be several reasons that a sister taxon relationship between Agnocardia and Afrocardium has never been posited. Both are poorly known taxa, represented by relatively few species, all of which are rare and often misidentified both in museum collections and in the literature. For instance, although Agnocardia had been reported from numerous localities in tropical America ( Vokes, 1984; Table 8), it was conspicuously unknown from Panama because all of the Agnocardia specimens examined by Woodring (1982) were misidentified as Trachycardium sp. Agnocardia has been reported almost exclusively from Old World fossils (in fact, Vokes, 1984; rejects all but one record of Old World Agnocardia ; Table 8) whereas Afrocardium is known mostly from Recent species from the relatively poorly studied Indian Ocean ( Table 3). Agnocardia has been studied almost exclusively by palaeontologists concerned with tropical American Palaeogene and Neogene biostratigraphy; Afrocardium by zoologists studying living Indo-Pacific faunas. It is highly probable that the palaeontologists studying Agnocardia never examined any species of Afrocardium , for Afrocardium was a tiny fragine from the Indian Ocean; likewise, the zoologists studying Afrocardium would not have examined any specimens of Agnocardia , because Agnocardia was a large extinct cardiine from the Americas. In both cases, these heavily ornamented cardiids were simply allied with whatever other heavily ornamented cardiids were already well-known from the region: Agnocardia was allied with the tropical American Trachycardium (or occasionally Acanthocardia, Miocene to Recent of Europe and known from the Miocene of Florida since Dall, 1900), whereas Afrocardium was allied with the Indo-Pacific fragines Fragum and Ctenocardia . Additionally, Trachycardium has long been a polyphyletic default taxon for large, heavily ornamented cardiids (see Discussions of Europicardium and Hedecardium , above), while Fragum has similarly been a polyphyletic default taxon for small, heavily ornamented and trigonally shaped cardiids (see Schneider, 1998a).

The biogeography of the sister taxa Agnocardia and Afrocardium is most unusual, with one taxon known mostly from the tropical Americas and the other mostly known from the Indian Ocean. This disjunct distribution originally led me to consider that Afrocardium had arrived in the Indian Ocean (by either dispersal or vicariance) without leaving a fossil record in Africa, hardly implausible given that Afrocardium is small and rare, and that Neogene marine fossiliferous strata in Africa are uncommon and understudied. Afrocardium would then be some sort of living fossil, a taxon with American affinities finding refuge in the Indian Ocean. Given that the systematics of the benthic marine invertebrate fauna of the Indian Ocean has been little studied since the early twentieth century, when usually taxonomic categories were much broader (eight of the nine Recent species of Afrocardium were originally classified simply as Cardium and le Tomlin, [1931] was the last person to pay virtually any attention to these species since Sowerby [1914]), perhaps modern systematic revisions of the marine invertebrates of the Indian Ocean would prove this region to be a biogeographical refuge in the sense that deeper waters and high latitudes are refugia ( Vermeij, 1987; Bottjer & Jablonski, 1988; Schneider & Marincovich, 2000).

However, I have identified three species of Afrocardium which may eliminate this biogeographical and stratigraphic conundrum: (1) Laevicardium (Plagiocardium) infinum Glibert, 1936 , from the Lower Bartonian (Middle Eocene) Sables de Wemmel of Belgium (2) Cardium defrancii Deshayes, 1858 from the Lower Oligocene of France, and (3) Cardium hirsutum Bronn, 1831 , from the Miocene of France, Austria, Hungary and Ukraine, Miocene and Pliocene of Italy, and Pliocene of Algeria ( Table 3) ( Monegatti & Raffi [2001] report Pleistocene Parvicardium hirsutum in a faunal list). Although the details of the phylogenetic relationships and biogeographical patterns amongst all the living and extinct species of Agnocardia and Afrocardium must await a species-level analysis, it appears that Agnocardia + Afrocardium is a tropical Tethyan clade which happened to become best known from its representatives in the Eocene to Pliocene of tropical America and the Recent of the Indian Ocean. Apparently, Afrocardium entered what is now the Indian Ocean when it was part of the Tethys seaway, and did not disperse from the western Atlantic. Until their species-level relationships are better resolved, Agnocardia and Afrocardium should be considered separate genera.

These three extinct species of Afrocardium had been identified by European palaeontologists as Plagiocardium or occasionally Parvicardium ( Sacco, 1899; Dautzenberg in Cerulli-Irelli, 1908; Lamothe, 1908; Dollfuss & Dautzenberg, 1913; Glibert, 1936; Glibert & van de Poel, 1970; Popov, 1977; Nevesskaia et al., 1993; Monegatti & Raffi, 2001). Just as species of Agnocardia were often identified as Trachycardium, and Afrocardium was classified as a subgenus of Fragum or Ctenocardia , European palaeontologists may simply have classified Laevicardium (Plagiocardium) infinum , Cardium hirsutum and C. defrancii as species of Plagiocardium because Plagiocardium was a small, heavily ornamented cardiid already known from the Palaeocene through Miocene of Europe.

An additional fossil species of Afrocardium is Cardium (Trachycardium) infantule Nomura & Zinbo, 1934 , from the Pleistocene of the Ryukyu Islands. The shell shape of this species is round, unlike Fraginae (and all Recent species of Afrocardium except for A. exochum ) and not dissimilar to Trachycardium (and Agnocardia , species of which are often classified as Trachycardium). Nomura & Zinbo (1934) therefore thought they were dealing with a species of Trachycardium; its small size was attributed to the specimens representing juveniles, hence the specific epithet infantule .

Figures

Figure 10. External views of right valves. A, Hedecardium (Hedecardium) waitakiense (DSIRGS 10837), hedeform shell shape. Scale bar = 10 mm. B, Freneixicardia verrucosa (NHM L7962), circular shell shape. Scale bar = 5 mm. Arrow indicates set of imbricated spines.

Figure 23. External view of left valves. A, adult of Loxocardium obliquum (FMNH PE3642). B, juvenile of Europicardium multicostatum (NHM PI TB6). Note loxofrom shell shape of A and B. C, adult of Europicardium multicostatum (NHM L8760), europiform shell shape. All scale bars = 1 mm.

Figure 26. Posterior slope of right valve of Hedecardium (Hedecardium) waitakiense (DSIRGS 10837). A, dorsalmost region of posterior slope. Arrow on right of figure indicates change in ribbing pattern between central slope and posterior slope. Arrow on left of figure indicates small simple spines on top of radial ribs. Scale bar = 5 mm. B, same specimen as in A, view more toward ventral margin; posterior margin visible at left of figure. Larger arrow indicates change in ribbing pattern between central and posterior slopes. Smaller arrow indicates small spine on top of rib. This rib and the next two posteriormost ribs display the eucardiid feature of a primary radial thread (see Schneider, 1998a). Scale bar = 7 mm.

Figure 27. Hedecardium (Iheringicardium). A, ventral margin of right valve of H. (I) patagonicum (NHM PI TB4). White arrows indicate interspaces in which secondary radial threads are visible. Black arrows indicate primary radial threads on top of ribs. Scale bar = 10 mm. B, ventral margin of left valve of H. (I) philippii (NHM PI TB1). Arrow points to doubled rib. Scale in mm indicated on figure. C, external view of left valve of H. (I) ameghinoi (NHM L12549), hedeform shell shape. Arrows point to doubled ribs. Scale bar = 10 mm. D, closeup of ventral margin of same specimen as in C. Arrow points to